diff --git a/package-lock.json b/package-lock.json
index a0928c02a1b..50178962a97 100644
--- a/package-lock.json
+++ b/package-lock.json
@@ -18401,6 +18401,7 @@
         "glob": "^12.0.0",
         "google-auth-library": "^9.11.0",
         "html-to-text": "^9.0.5",
+        "http-proxy-agent": "^7.0.2",
         "https-proxy-agent": "^7.0.6",
         "ignore": "^7.0.0",
         "ipaddr.js": "^1.9.1",
diff --git a/packages/core/package.json b/packages/core/package.json
index b6a26d0db86..3a65b0c5e5e 100644
--- a/packages/core/package.json
+++ b/packages/core/package.json
@@ -67,6 +67,7 @@
     "glob": "^12.0.0",
     "google-auth-library": "^9.11.0",
     "html-to-text": "^9.0.5",
+    "http-proxy-agent": "^7.0.2",
     "https-proxy-agent": "^7.0.6",
     "ignore": "^7.0.0",
     "ipaddr.js": "^1.9.1",
diff --git a/packages/core/src/core/contentGenerator.test.ts b/packages/core/src/core/contentGenerator.test.ts
index 4efd9f65c6e..9e770564449 100644
--- a/packages/core/src/core/contentGenerator.test.ts
+++ b/packages/core/src/core/contentGenerator.test.ts
@@ -13,6 +13,8 @@ import {
 } from './contentGenerator.js';
 import { createCodeAssistContentGenerator } from '../code_assist/codeAssist.js';
 import { GoogleGenAI } from '@google/genai';
+import { HttpProxyAgent } from 'http-proxy-agent';
+import { HttpsProxyAgent } from 'https-proxy-agent';
 import type { Config } from '../config/config.js';
 import { LoggingContentGenerator } from './loggingContentGenerator.js';
 import { loadApiKey } from './apiKeyCredentialStorage.js';
@@ -424,6 +426,174 @@ describe('createContentGenerator', () => {
     );
   });
 
+  it('should inject HttpsProxyAgent into googleAuthOptions when proxy URL uses https://', async () => {
+    const mockConfigWithProxy = {
+      getModel: vi.fn().mockReturnValue('gemini-pro'),
+      getProxy: vi.fn().mockReturnValue('https://proxy.example.com:8080'),
+      getUsageStatisticsEnabled: () => false,
+      getClientName: vi.fn().mockReturnValue(undefined),
+    } as unknown as Config;
+
+    const mockGenerator = {
+      models: {},
+    } as unknown as GoogleGenAI;
+    vi.mocked(GoogleGenAI).mockImplementation(() => mockGenerator);
+
+    await createContentGenerator(
+      {
+        apiKey: 'test-api-key',
+        vertexai: true,
+        authType: AuthType.USE_VERTEX_AI,
+        proxy: 'https://proxy.example.com:8080',
+      },
+      mockConfigWithProxy,
+    );
+
+    expect(GoogleGenAI).toHaveBeenCalledWith(
+      expect.objectContaining({
+        googleAuthOptions: {
+          clientOptions: {
+            transporterOptions: {
+              agent: expect.any(HttpsProxyAgent),
+            },
+          },
+        },
+      }),
+    );
+  });
+
+  it('should still use HttpsProxyAgent for HTTPS destinations even when proxy URL uses http://', async () => {
+    const mockConfigWithProxy = {
+      getModel: vi.fn().mockReturnValue('gemini-pro'),
+      getProxy: vi.fn().mockReturnValue('http://proxy.example.com:8080'),
+      getUsageStatisticsEnabled: () => false,
+      getClientName: vi.fn().mockReturnValue(undefined),
+    } as unknown as Config;
+
+    const mockGenerator = {
+      models: {},
+    } as unknown as GoogleGenAI;
+    vi.mocked(GoogleGenAI).mockImplementation(() => mockGenerator);
+
+    await createContentGenerator(
+      {
+        apiKey: 'test-api-key',
+        vertexai: true,
+        authType: AuthType.USE_VERTEX_AI,
+        proxy: 'http://proxy.example.com:8080',
+      },
+      mockConfigWithProxy,
+    );
+
+    expect(GoogleGenAI).toHaveBeenCalledWith(
+      expect.objectContaining({
+        googleAuthOptions: {
+          clientOptions: {
+            transporterOptions: {
+              agent: expect.any(HttpsProxyAgent),
+            },
+          },
+        },
+      }),
+    );
+  });
+
+  it('should inject HttpProxyAgent when destination baseUrl uses http://', async () => {
+    const mockConfigWithProxy = {
+      getModel: vi.fn().mockReturnValue('gemini-pro'),
+      getProxy: vi.fn().mockReturnValue('http://proxy.example.com:8080'),
+      getUsageStatisticsEnabled: () => false,
+      getClientName: vi.fn().mockReturnValue(undefined),
+    } as unknown as Config;
+
+    const mockGenerator = {
+      models: {},
+    } as unknown as GoogleGenAI;
+    vi.mocked(GoogleGenAI).mockImplementation(() => mockGenerator);
+
+    vi.stubEnv('GOOGLE_VERTEX_BASE_URL', 'http://localhost:9999');
+
+    await createContentGenerator(
+      {
+        apiKey: 'test-api-key',
+        vertexai: true,
+        authType: AuthType.USE_VERTEX_AI,
+        proxy: 'http://proxy.example.com:8080',
+      },
+      mockConfigWithProxy,
+    );
+
+    expect(GoogleGenAI).toHaveBeenCalledWith(
+      expect.objectContaining({
+        googleAuthOptions: {
+          clientOptions: {
+            transporterOptions: {
+              agent: expect.any(HttpProxyAgent),
+            },
+          },
+        },
+      }),
+    );
+  });
+
+  it('should trim whitespace from proxy URL before instantiating agent', async () => {
+    const mockConfigWithProxy = {
+      getModel: vi.fn().mockReturnValue('gemini-pro'),
+      getProxy: vi.fn().mockReturnValue('  https://proxy.example.com:8080  '),
+      getUsageStatisticsEnabled: () => false,
+      getClientName: vi.fn().mockReturnValue(undefined),
+    } as unknown as Config;
+
+    const mockGenerator = {
+      models: {},
+    } as unknown as GoogleGenAI;
+    vi.mocked(GoogleGenAI).mockImplementation(() => mockGenerator);
+
+    await createContentGenerator(
+      {
+        apiKey: 'test-api-key',
+        vertexai: true,
+        authType: AuthType.USE_VERTEX_AI,
+        proxy: '  https://proxy.example.com:8080  ',
+      },
+      mockConfigWithProxy,
+    );
+
+    expect(GoogleGenAI).toHaveBeenCalledWith(
+      expect.objectContaining({
+        googleAuthOptions: {
+          clientOptions: {
+            transporterOptions: {
+              agent: expect.any(HttpsProxyAgent),
+            },
+          },
+        },
+      }),
+    );
+  });
+
+  it('should not include googleAuthOptions when no proxy is configured', async () => {
+    const mockGenerator = {
+      models: {},
+    } as unknown as GoogleGenAI;
+    vi.mocked(GoogleGenAI).mockImplementation(() => mockGenerator);
+
+    await createContentGenerator(
+      {
+        apiKey: 'test-api-key',
+        vertexai: true,
+        authType: AuthType.USE_VERTEX_AI,
+      },
+      mockConfig,
+    );
+
+    const callArg = vi.mocked(GoogleGenAI).mock.calls[0][0] as Record<
+      string,
+      unknown
+    >;
+    expect(callArg).not.toHaveProperty('googleAuthOptions');
+  });
+
   it('should pass api key as Authorization Header when GEMINI_API_KEY_AUTH_MECHANISM is set to bearer', async () => {
     const mockConfig = {
       getModel: vi.fn().mockReturnValue('gemini-pro'),
diff --git a/packages/core/src/core/contentGenerator.ts b/packages/core/src/core/contentGenerator.ts
index bcee8cfef4b..1e24e16eff0 100644
--- a/packages/core/src/core/contentGenerator.ts
+++ b/packages/core/src/core/contentGenerator.ts
@@ -13,6 +13,8 @@ import {
   type EmbedContentResponse,
   type EmbedContentParameters,
 } from '@google/genai';
+import { HttpProxyAgent } from 'http-proxy-agent';
+import { HttpsProxyAgent } from 'https-proxy-agent';
 import * as os from 'node:os';
 import { createCodeAssistContentGenerator } from '../code_assist/codeAssist.js';
 import { isCloudShell } from '../ide/detect-ide.js';
@@ -336,11 +338,25 @@ export async function createContentGenerator(
         httpOptions.baseUrl = baseUrl;
       }
 
+      const proxyUrl = config.proxy?.trim();
+      const proxyAgent = proxyUrl
+        ? baseUrl?.startsWith('http://')
+          ? new HttpProxyAgent(proxyUrl)
+          : new HttpsProxyAgent(proxyUrl)
+        : undefined;
+
       const googleGenAI = new GoogleGenAI({
         apiKey: config.apiKey === '' ? undefined : config.apiKey,
         vertexai: config.vertexai ?? config.authType === AuthType.USE_VERTEX_AI,
         httpOptions,
         ...(apiVersionEnv && { apiVersion: apiVersionEnv }),
+        ...(proxyAgent && {
+          googleAuthOptions: {
+            clientOptions: {
+              transporterOptions: { agent: proxyAgent },
+            },
+          },
+        }),
       });
       return new LoggingContentGenerator(googleGenAI.models, gcConfig);
     }